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Like United States Numbered Highways and many national routing systems, the U.S. Bicycle Route system is designed to roughly follow a grid. Mainline routes are the major cross-country routes and are represented with one- or two-digit numbers. Even-numbered routes are planned to primarily run east-west, with low-numbered routes in the north and high-numbered routes in the south. Odd-numbered routes will primarily run north-south, with low-numbered routes starting in the east and ascending in number toward the west. Three-digit numbers are assigned to auxiliary routes, with the last two digits denoting the parent that the auxiliary connects to. Much like other routing systems, the grid is sometimes violated; for example, U.S. Bicycle Route 76 (USBR 76) is projected to turn to the north in Colorado and end in Oregon as opposed to California, south of (and temporarily concurrent with) USBR 20 but far north of USBR 50.

The existing USBR 1 will be the easternmost route, though USBR 5 will run farther east of it in Virginia and the Carolinas. The westernmost and northernmost routes are USBR 97 and USBR 8, respectively, both of which are in the State of Alaska. Outside of Alaska, the westernmost route is expected to be USBR 95 and the northernmost USBR 10. USBR 90 is expected to be the southernmost route.[6] Despite the analogy the system has to the U.S. Highway system, the USBRS's route numbers do not necessarily trace the same route as the corresponding U.S. Highway number; for example, while USBR 1 will run close to the East Coast and thus parallel U.S. Route 1 (US 1), the projected route of USBR 10 generally follows US 2.

In order for a route to qualify as a U.S. Bike Route, it needs to connect two or more states, connect multiple U.S. Bike Routes, or connect a U.S. Bike Route with a national border.

AASHTO established a new task force in 2003 to study expansion of the system.[2][8][9] The task force included state and federal highway officials and representatives from bicycling organizations. In October 2008, AASHTO approved a national-level corridor and route designation plan.[10] Other organizations involved in the effort include state departments of transportation, the Federal Highway Administration, and the Adventure Cycling Association.

In 2009, the U.S. House of Representatives proposed moving the U.S. Bicycle Route System under the authority of the Federal Highway Administration as part of a new Office of Livability.[11]

In early May 2011, the first major expansion of the system was made. Five new parent routes, two child routes, and one alternate route were created, along with modifications to the existing routes in Virginia and the establishment of USBR 1 in New England.[3][4]

Across 2013, several other additions to the system were made. After approval in 2012, signage for USBR 45 in Minnesota was completed in the summer. An expansion of USBR 76 into Missouri was signed in October, and both Tennessee and Maryland entered the system on November 5 with USBR 23 and USBR 50, respectively.[5] Florida has also begun planning on four bicycle routes, including its stretch of USBR 1 and USBR 90.[12]

As of May 2014, 14 parent routes officially exist, so most of the items listed below are presently defined only as "Prioritized Corridors" which are "50-mile wide areas where a route may be developed."[6]Subsidiary routes, of which only three currently exist, are grouped with their one- or two-digit parent. Approved or signed routes are currently located in the District of Columbia and 16 states: Alaska, Florida, Kentucky, Illinois, Maine, Maryland, Massachusetts, Michigan, Minnesota, Missouri, New Hampshire, North Carolina, Ohio, Tennessee, Virginia, and Washington. Alaska has the most of any state, with six active routes in total.

One of the two original routes, this is planned to be expanded to the longest route, running from the existing eastern terminus near the Atlantic Ocean in Virginia west to the Pacific Ocean west of Eugene, Oregon. The number refers to 1776 and the U.S. bicentennial year 1976 when this was the "Bikecentennial" route. Like USBR 1, unofficial signs exist in places along the route, which is officially only from Virginia to Missouri. Route approved and signed in Missouri in October 2013.[20]